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Brood Size and Sex Ratio in Response to Host Quality and Wasp Traits in the Gregarious Parasitoid Oomyzus Sokolowskii (Hymenoptera: Eulophidae)

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Brood Size and Sex Ratio in Response to Host Quality and Wasp Traits in the Gregarious Parasitoid Oomyzus Sokolowskii (Hymenoptera: Eulophidae) Brood size and sex ratio in response to host quality and wasp traits in the gregarious parasitoid Oomyzus sokolowskii (Hymenoptera: Eulophidae) Xianwei Li, Liangting Zhu, Ling Meng and Baoping Li School of Plant Protection, Nanjing Agricultural University, Nanjing, Jiangsu, China ABSTRACT This laboratory study investigated whether the larval-pupal parasitoid Oomyzus sokolowskii females adjust their brood size and sex ratio in response to body size and stage of Plutella xylostella larval hosts, as well as to their own body size and the order of oviposition. These factors were analyzed using multiple regression with simultaneous entry of them and their two-way interactions. Parasitoids brood size tended to increase with host body size at parasitism when the 4th instar larval host was attacked, but did not change when the 2nd and 3rd instar larvae were attacked. Parasitoids did not vary in brood size according to their body size, but decreased with their bouts of oviposition on a linear trend from 10 offspring adults emerged per host in the first bout of oviposition down to eight in the third. Parasitoid offspring sex ratio did not change with host instar, host body weight, wasp body size, and oviposition bout. Proportions of male offspring per brood were from 11% to 13% from attacking the 2nd to 4th instar larvae and from 13% to 16% across three successive bouts of oviposition, with a large variation for smaller host larvae and wasps. When fewer than 12 offspring were emerged from a host, one male was most frequently produced; when more than 12 offspring were emerged, two or more males were produced. Our study suggests that O. sokolowskii females may optimize their clutch size in response to body size of mature P. xylostella larvae, and their sex allocation in response to clutch size. Submitted 3 August 2016 Accepted 17 December 2016 Subjects Animal Behavior, Entomology Published 24 January 2017 Keywords Sex allocation, Plutella xylostella, Sex ratio, Clutch size, Oviposition behavior Corresponding author Baoping Li, [email protected] Academic editor INTRODUCTION Leon Higley Parasitoids make oviposition decisions depending on a variety of factors, including the Additional Information and Declarations can be found on quality of hosts and characteristics of ovipositing wasps (Charnov et al., 1981; Van Alphen & page 9 Visser, 1990; Godfray, 1994; Ellers & Jervis, 2003). Host quality for parasitoid development DOI 10.7717/peerj.2919 is often assumed to scale with host size and this pattern is true for idiobiont parasitoids, Copyright which arrest host growth at the time of oviposition (Askew & Shaw, 1986; King, 1990; Otto 2017 Li et al. & Mackauer, 1998). This pattern, however, may not be universally applicable to koinobiont Distributed under parasitoids, which allow the host to continue to develop after it has been parasitized (Werren, Creative Commons CC-BY 4.0 1984; Waage, 1986; Mackauer, Sequeira & Otto, 1997; Harvey, Sano & Tanaka, 2010), and thus the future resources for developing koinobiont larvae can vary depending on the host OPEN ACCESS How to cite this article Li et al. (2017), Brood size and sex ratio in response to host quality and wasp traits in the gregarious parasitoid Oomyzus sokolowskii (Hymenoptera: Eulophidae). PeerJ 5:e2919; DOI 10.7717/peerj.2919 age or development stage at the time of oviposition (Harvey & Strand, 2002; Harvey, 2005), though there are some koinobiont parasitoids still preferring larger body hosts (King, 1989; Elzinga, Harvey & Biere, 2003; Kant, Minor & Trewick, 2012). In addition to host quality, parasitoid oviposition decisions may also depend on characteristics of ovipositing wasps, including their body size and states, such as egg load, age, and nutrition states. The wasp size is frequently considered to be the main target for selection (Godfray, 1994; Ode & Strand, 1995; Bezemer, Harvey & Mills, 2005). It can affect fitness by influencing searching efficiency, longevity, or egg supplies (Mayhew & Heitmans, 2000; Milonas, 2005; Jervis, Ellers & Harvey, 2008; Kasamatsu & Abe, 2015). In addition, it may also influence the quality of host attacked, in that a small female wasp may not be able to use a large, good quality host that is more effective in defense against attacks (Godfray, 1994; Henry, Ma & Roitberg, 2009). Parasitoid state can affect many parasitoid behaviors (Van Alphen & Visser, 1990; Roitberg & Bernhard, 2008; Harvey, Poelman & Tanaka, 2013). For example, oviposition experience and physiological constraints, such as egg load, can influence parasitoid oviposition decisions (Cloutier et al., 1991; Henneman et al., 1995; Sirot, Ploye & Bernstein, 1997; Ueno, 1999; Rosenheim et al., 2008; Dieckhoff et al., 2014). Therefore, parasitoids may integrate the information provided by a variety of cues about hosts and themselves to make oviposition decisions. Oomyzus sokolowskii (Kurdjumov) is a gregarious larval-pupal koinobiont endopara- sitoid of the diamondback moth, Plutella xylostella (L.) (Talekar & Shelton, 1993; Talekar & Hu, 1996; Silva-Torres et al., 2009), which is one of major herbivorous pests on cruciferous crops (Furlong & Zalucki, 2007; Zalucki et al., 2012; Li et al., 2016). Because P. xylostella populations have developed resistance to numerous pesticides (Liu, Tzeng & Sun, 1981; Ferré et al., 1991; Li et al., 2006), biological control with natural enemies offers greater potential (Talekar & Shelton, 1993; Delvare, 2004; Sarfraz, Keddie & Dosdall, 2005). The parasitoid O. sokolowskii has been found parasitizing P. xylostella worldwide (Wang et al., 1999; Nakamura & Noda, 2001; Silva-Torres et al., 2009; Li, Niu & Liu, 2014), showing the potential for biological control of P. xylostella (Talekar & Hu, 1996; Furlong, Wright & Dosdall, 2013). For O. sokolowskii developmental performances in attacking P. xylostella larvae of different instars, two non-choice studies are not consistent in their conclusions, though the female wasp prefers mature larvae under choice circumstances (Talekar & Hu, 1996). While Wang et al. (1999) showed similar performances in the development time, number, and sex ratio of offspring in attacking host larvae of different instars, Nakamura & Noda (2002) showed that O. sokolowskii brood size increased with host body size when hosts for parasitism were confined to the prepupal stage. It would be interesting to examine whether or not parasitoid brood size varies as a function of host body size depending on host larval stage at parasitism. In addition, states of ovipositing wasps may influence oviposition decisions. It has been shown that older O. sokolowskii females declined in the progeny produced per female and the number of parasitoids emerged per host (Silva-Torres, Barros & Torres, 2009; Sow et al., 2013). However, scant attention has been paid to the effect of O. sokolowskii female body size on its oviposition behavior. Therefore, to fully understand O. sokolowskii oviposition strategy, we need studies involving both host quality and wasp traits. Li et al. (2017), PeerJ, DOI 10.7717/peerj.2919 2/14 This laboratory study aimed to answer the question: how do O. sokolowskii females make oviposition decisions on brood size and sex ratio in response to both host quality and their own traits? We examined combined effects of body size and age of P. xylostella larvae as well as body size and ovipositing order of the female wasp, by using mutiple regression models with simultaneous entry of these factors and their two-way interactions. Our study provides new data to the understanding of oviposition behavior in gregarious parasitoids. MATERIALS & METHODS Insects Plutella xylostella was collected in the early spring 2014 from a pakchoi (Brassica chinensis L.) field on eastern suburb of Nanjing, Jiangsu, and thereafter maintained on potted pakchoi seedlings in insectary at 25 ± 1 ◦C, 60 ± 5% RH, and a photoperiod of 16:8 h (L:D). Oomyzus sokolowskii was obtained from the Key Laboratory of Northwest Loess Plateau Crop Pest Management of Ministry of Agriculture of China, Northwest A&F University, Yangling, Shaanxi. It was maintained with P. xylostella 4th instar larvae as hosts in the insec- tary. A group of four host larvae was introduced into a 4 ml centrifuge tube, which was cov- ered by 100 mesh plastic screen for ventilation and supplied with a piece of fresh pakchoi leaf as food. Then a female O. sokolowskii was released into the tube. After 24 h the larvae were removed from the tube and transferred individually to 10-cm-diameter Petri dishes con- taining excised fresh pakchoi leaves, which were replaced daily. The host pupae parasitized (different from normal ones by dark body color) were collected in groups in vials, where emerged parasitoid adults were maintained for one day to ensure fully mating. Naive females emerged within one day were used in the experiments. Oviposition behavior Plutella xylostella 2nd, 3rd and 4th instar larvae were used as hosts. Each larva was individually exposed to parasitism after weighed (AL204-IC, with the measurement accuracy of 0.01 mg; Mettler Toledo, Columbus, OH, USA). After introduced into a 4 ml centrifuge tube containing a host larva, a female wasp was continuously observed until a bout of oviposition was completed. The wasp then was removed and immediately introduced into another tube containing a same-aged host larva for the second bout of oviposition, and then for the third. Three successive bouts of oviposition took ca. 5–6 h to be accomplished by a wasp, which was considered as a replicate. The number
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